Advertisement

Geographic and Temporal Variation of Distinct Intracellular Endosymbiont Strains of Wolbachia sp. in the Grasshopper Chorthippus parallelus: a Frequency-Dependent Mechanism?

  • Paloma Martínez-Rodríguez
  • Emilio Rolán-Alvarez
  • M. del Mar Pérez-Ruiz
  • Francisca Arroyo-Yebras
  • Carla Carpena-Catoira
  • Antonio Carvajal-Rodríguez
  • José L. BellaEmail author
Genes and Genomes

Abstract

Wolbachia is an intracellular endosymbiont that can produce a range of effects on host fitness, but the temporal dynamics of Wolbachia strains have rarely been experimentally evaluated. We compare interannual strain frequencies along a geographical region for understanding the forces that shape Wolbachia strain frequency in natural populations of its host, Chorthippus parallelus (Orthoptera, Acrididae). General linear models show that strain frequency changes significantly across geographical and temporal scales. Computer simulation allows to reject the compatibility of the observed patterns with either genetic drift or sampling errors. We use consecutive years to estimate total Wolbachia strain fitness. Our estimation of Wolbachia fitness is significant in most cases, within locality and between consecutive years, following a negatively frequency-dependent trend. Wolbachia spp. B and F strains show a temporal pattern of variation that is compatible with a negative frequency-dependent natural selection mechanism. Our results suggest that such a mechanism should be at least considered in future experimental and theoretical research strategies that attempt to understand Wolbachia biodiversity.

Keywords

Fitness estimate Frequency-dependent natural selection Temporal biodiversity Evolutionary dynamics 

Notes

Acknowledgements

We thank Dr. P.L. Mason (University of Glasgow) for his comments and suggestions as well as the constructive comments of our referees. This work was supported by the Spanish Ministerio de Economía y Competitividad (CGL2016-75482-P and BFU2013-44635 grants) with the collaboration of Chromacell S.L. We are grateful to the many people who helped in the collection and handling of the grasshoppers and to the other members of our groups. We also express our gratitude to the Aragón Government, Spain, and the French Parc National des Pyrénées for permission to collect the grasshoppers.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2019_1338_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1601 kb)

References

  1. 1.
    Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7:e38544CrossRefGoogle Scholar
  2. 2.
    LePage D, Bordenstein SR (2013) Wolbachia: can we save lives with a great pandemic? Trends Parasitol 29:385–393CrossRefGoogle Scholar
  3. 3.
    Ros VID, Fleming VM, Feil EJ, Breeuwer JAJ (2009) How diverse is the genus Wolbachia?. Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Appl Environ Microbiol 75:1036–1043CrossRefGoogle Scholar
  4. 4.
    Gerth M, Gansauge MT, Weigert A, Bleidorn C (2014) Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat Commun 5:5117CrossRefGoogle Scholar
  5. 5.
    Bordenstein SR, Werren JH (1998) Effects of A and B Wolbachia and host genotype on interspecies cytoplasmic incompatibility in Nasonia. Genetics 148:1833–1844Google Scholar
  6. 6.
    Bordenstein SR, O'Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409:707–710CrossRefGoogle Scholar
  7. 7.
    Telschow A, Hammerstein P, Werren JH (2005) The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59:1607–1619CrossRefGoogle Scholar
  8. 8.
    Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190CrossRefGoogle Scholar
  9. 9.
    Gazla I, Carracedo M (2011) Wolbachia induces sexual isolation in Drosophila melanogaster and Drosophila simulans.Open J Genet 1:18–26CrossRefGoogle Scholar
  10. 10.
    Ringo J, Sharon G, Segal D (2011) Bacteria-induced sexual isolation in Drosophila. Fly 5:310–315CrossRefGoogle Scholar
  11. 11.
    Brucker RM, Bordenstein SR (2012) The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66:349–362CrossRefGoogle Scholar
  12. 12.
    Brucker RM, Bordenstein SR (2012) Speciation by symbiosis. Trends Ecol Evol 27:443–451CrossRefGoogle Scholar
  13. 13.
    Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707CrossRefGoogle Scholar
  14. 14.
    Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751CrossRefGoogle Scholar
  15. 15.
    Merçot H, Poinsot D (2009) Infection by Wolbachia: from passengers to residents. C R Biol 332:284–297CrossRefGoogle Scholar
  16. 16.
    Saridaki A, Bourtzis K (2010) Wolbachia: more than just a bug in insects genitals. Curr Opin Microbiol 13:67–72CrossRefGoogle Scholar
  17. 17.
    Dillon RJ, Webster G, Weightman AJ, Dillon VM, Blanford S, Charnley AK (2008) Composition of Acridid gut bacterial communities as revealed by 16S rRNA gene analysis. J Invertebr Pathol 97:265–272CrossRefGoogle Scholar
  18. 18.
    Martínez P, Del Castillo P, Bella JL (2009) Cytological detection of Wolbachia in squashed and paraffin embedded insect tissues. Biotech Histochem 84:347–353CrossRefGoogle Scholar
  19. 19.
    Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MC, Tettelin H, Werren JH (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72(11):7098–7110CrossRefGoogle Scholar
  20. 20.
    Bella JL, Martínez-Rodríguez P, Arroyo F, Bernal A, Sarasa J, Fernández-Calvín B, Mason PL, Zabal-Aguirre M (2010) Wolbachia infection in the Chorthippus parallelus hybrid zone: evidence for its role as a reproductive barrier. J Orthop Res 19:205–212CrossRefGoogle Scholar
  21. 21.
    Zabal-Aguirre M, Arroyo F, Bella JL (2010) Distribution of Wolbachia infection in Chorthippus parallelus populations within and beyond a Pyrenean hybrid zone. Heredity 104:174–184CrossRefGoogle Scholar
  22. 22.
    Martínez-Rodríguez P, Hernández-Pérez M, Bella JL (2013) Detection of Spiroplasma and Wolbachia in the bacterial gonad community of Chorthippus parallelus. Microb Ecol 66:211–223CrossRefGoogle Scholar
  23. 23.
    Martínez-Rodríguez P, Bella JL (2018) Chorthippus parallelus and Wolbachia: overlapping orthopteroid and bacterial hybrid zones. Front Genet 9:604.  https://doi.org/10.3389/fgene.2018.00604 CrossRefGoogle Scholar
  24. 24.
    Zabal-Aguirre M, Arroyo F, García-Hurtado J, de la Torre J, Hewitt GM, Bella JL (2014) Wolbachia effects in natural populations of Chorthippus parallelus from the Pyrenean hybrid zone. J Evol Biol 27:1136–1148CrossRefGoogle Scholar
  25. 25.
    Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2:17007CrossRefGoogle Scholar
  26. 26.
    Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  27. 27.
    Shuker DM, King TM, Bella JL, Butlin RK (2005) The genetic basis of speciation in a grasshopper hybrid zone. In: Fellowes M, Holloway G, Roff J (eds) Insect evolutionary biology. CABI Publishing, Oxford University Press, Wallingford, pp 427–454Google Scholar
  28. 28.
    Sarasa J, Bernal A, Fernández-Calvin B, Bella JL (2013) Wolbachia induced cytogenetical effects, as evidenced in Chorthippus parallelus (Orthoptera). Cytogenet Genome Res 139:36–43CrossRefGoogle Scholar
  29. 29.
    Funkhouser-Jones LJ, Sehnert SR, Martínez-Rodríguez P, Toribio R, Pita M, Bella JL, Bordenstein SR (2015) Wolbachia co-infection in a hybrid zone: discovery of horizontal gene transfers from two Wolbachia supergroups into an animal genome. Peer J. 3: e1479.CrossRefGoogle Scholar
  30. 30.
    Toribio-Fernández R, Bella JL, Martínez-Rodríguez P, Funkhouser-Jones LJ, Bordenstein SR, Pita M (2017) Chromosomal localization of Wolbachia inserts in the genomes of two subspecies of Chorthippus parallelus forming a Pyrenean hybrid zone. Chromosom Res 25:215–225CrossRefGoogle Scholar
  31. 31.
    Turelli M (1994) Evolution of incompatibility-inducing microbes and their hosts. Evolution 48:1500–1513CrossRefGoogle Scholar
  32. 32.
    Engelstädter J, Charlat S, Pomiankowski A, Hurst GDD (2006) The evolution of cytoplasmic incompatibility types: integrating segregation inbreeding and outbreeding. Genetics 172:2601–2611CrossRefGoogle Scholar
  33. 33.
    Hancock PA, Sinkins SP, Godfray HCJ (2011) Population dynamic models of the spread of Wolbachia. Am Nat 177:323–333CrossRefGoogle Scholar
  34. 34.
    Zug R, Koehncke A, Hammerstein P (2012) Epidemiology in evolutionary time: the case of Wolbachia horizontal transmission between arthropod host species. J Evol Biol 25:2149–2160CrossRefGoogle Scholar
  35. 35.
    Martínez-Rodríguez P, Granero-Belinchón R, Arroyo-Yebras F, Bella JL (2014) New insight into Wolbachia epidemiology: its varying incidence during the host life cycle can alter bacteria spread. Bull Math Biol 76:2646–2663CrossRefGoogle Scholar
  36. 36.
    Telschow A, Hilgenboecker K, Hammerstein P, Werren JH (2014) Dobzhansky-Muller and Wolbachia-induced incompatibilities in a diploid genetic system. PLoS One 9:e95488CrossRefGoogle Scholar
  37. 37.
    Merçot H, Charlat S (2004) Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120(1–3):51–59CrossRefGoogle Scholar
  38. 38.
    Duron O, Labbe P, Berticat C, Rousset F, Guillot S, Raymond M, Weill M (2006) High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoes. Evolution 60:303–314CrossRefGoogle Scholar
  39. 39.
    Duron O, Fort P, Weill M (2007) Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity 98:368–374CrossRefGoogle Scholar
  40. 40.
    Mouton L, Henri H, Charif D, Bouletrea M, Vavre F (2007) Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett 3:210–213CrossRefGoogle Scholar
  41. 41.
    Hurst GDD, Jiggins FM, Robinson SJW (2001) What causes inefficient transmission of male-killing Wolbachia in Drosophila? Heredity 87:220–226CrossRefGoogle Scholar
  42. 42.
    Perrot-Minnot MJ, Guo LR, Werren JH (1996) Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis: effects on compatibility. Genetics 143:961–972Google Scholar
  43. 43.
    Stevens L, Giordano R, Fialho RF (2001) Male-killing, nematode infections, bacteriophage infection, and virulence of cytoplasmic bacteria in the genus Wolbachia. Annu Rev Ecol Syst 32:519–545CrossRefGoogle Scholar
  44. 44.
    Tortosa P, Charlat S, Labbe P, Dehecq JS, Barre H, Weill M (2010) Wolbachia age-sex-specific density in Aedes albopictus: a host evolutionary response to cytoplasmic incompatibility? PLoS One 5:e9700CrossRefGoogle Scholar
  45. 45.
    Xie RR, Zhou LL, Zhao ZJ, Hong XY (2010) Male age influences the strength of Cardinium-induced cytoplasmic incompatibility expression in the carmine spider mite Tetranychus cinnabarinus. Appl Entomol Zool 45:417–423CrossRefGoogle Scholar
  46. 46.
    Chevalier F, Herbinière-Gaboreau J, Bertaux J, Raimond M, Morel F, Bouchon D, Grève P, Braquart-Varnier C (2011) The immune cellular effectors of terrestrial isopod Armadillidium vulgare: meeting with their invaders, Wolbachia. PLoS One 6:e18531CrossRefGoogle Scholar
  47. 47.
    Wong ZS, Hedges LM, Brownlie JC, Johnson KN (2011) Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS One 6:e25430CrossRefGoogle Scholar
  48. 48.
    Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338Google Scholar
  49. 49.
    Marcade I, Souty-Grosset C, Bouchon D, Rigaud T, Raimond R (1999) Mitochondrial DNA variability and Wolbachia infection in two sibling woodlice species. Heredity 83:71–78CrossRefGoogle Scholar
  50. 50.
    Narita S, Nomura M, Kageyama D (2007) Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: transmission efficiencies and population density dynamics of each Wolbachia strain. FEMS Microbiol Ecol 61:235–245CrossRefGoogle Scholar
  51. 51.
    Frank SA (1998) Dynamics of cytoplasmic incompatability with multiple Wolbachia infections. J Theor Biol 192:213–218CrossRefGoogle Scholar
  52. 52.
    Telschow A, Hammerstein P, Werren JH (2002) The effect of Wolbachia on genetic divergence between populations: models with two-way migration. Am Nat 160:S54–S66Google Scholar
  53. 53.
    Telschow A, Hammerstein P, Werren JH (2002) Effects of Wolbachia on genetic divergence between populations: mainland-island model. Integr Comp Biol 42:340–351CrossRefGoogle Scholar
  54. 54.
    Engelstädter J, Telschow A, Hammerstein P (2004) Infection dynamics of different Wolbachia-types within one host population. J Theor Biol 231:345–355CrossRefGoogle Scholar
  55. 55.
    Telschow A, Yamamura N, Werren JH (2005) Bidirectional cytoplasmic incompatibility and the stable coexistence of two Wolbachia strains in parapatric host populations. J Theor Biol 235:265–274CrossRefGoogle Scholar
  56. 56.
    Telschow A, Engelstädter J, Yamamura N, Hammerstein P, Hurst GDD (2006) Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J Evol Biol 19:869–878CrossRefGoogle Scholar
  57. 57.
    Telschow A, Flor M, Kobayashi Y, Hammerstein P, Werren JH (2007) Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model. PLoS One 2:e701CrossRefGoogle Scholar
  58. 58.
    Flor M, Hammerstein P, Telschow A (2007) Wolbachia-induced unidirectional cytoplasmic incompatibility and the stability of infection polymorphism in parapatric host populations. J Evol Biol 20:696–706CrossRefGoogle Scholar
  59. 59.
    Engelstädter J, Telschow A (2009) Cytoplasmic incompatibility and host population structure. Heredity 103:196–207CrossRefGoogle Scholar
  60. 60.
    Dobson SL, Rattanadechakul W, Marsland EJ (2004) Fitness advantage and cytoplasmic incompatibility in Wolbachia single- and superinfected Aedes albopictus. Heredity 93:135–142CrossRefGoogle Scholar
  61. 61.
    Brelsfoard CL, Dobson SL (2011) Wolbachia effects on host fitness and the influence of male aging on cytoplasmic incompatibility in Aedes polynesiensis (Diptera: Culicidae). J Med Entomol 48:1008–1015CrossRefGoogle Scholar
  62. 62.
    Joshi D, McFadden MJ, Bevins B, Zhangand F, Xi Z (2014) Wolbachia strain wAlbB confers both fitness costs and benefit on Anopheles stephensi. Parasit Vectors 7:336–345CrossRefGoogle Scholar
  63. 63.
    Cattel J, Kaur R, Gibert P, Martínez J, Raimout A, Jiggins F, Andrieux T, Siozios S, Anfora G, Miller W, Rota-Stabelli O, Mouton L (2016) Wolbachia in European populations of the invasive pest Drosophila suzukii: regional variation in infection frequencies. PLoS One.  https://doi.org/10.1371/journal.pone.0147766
  64. 64.
    Hamm CA, Begun DJ, Vo A, Smith CCR, Saelao P, Shaver AO, Jaenike J, Turelli M (2014) Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol Ecol 23:4871–4885CrossRefGoogle Scholar
  65. 65.
    Atyame CM, Labbé P, Rousset F, Beji M, Makoundou P, Duron O, Dumas E, Pasteur N, Bouattour A, Fort P, Weill M (2015) Stable coexistence of incompatible Wolbachia along a narrow contact zone in mosquito field populations. Mol Ecol 24:508–521CrossRefGoogle Scholar
  66. 66.
    Charlesworth B, Charlesworth D (2010) Elements of evolutionary genetics. Roberts & Company Publishers, ColoradoGoogle Scholar
  67. 67.
    Chrostek E, Pelz-Stelinski K, Hurst GDD, Hughes GL (2017) Horizontal transmission of intracellular insect symbionts via plants. Front Microbiol 8:2237CrossRefGoogle Scholar
  68. 68.
    Virdee SR, Hewitt GM (1990) Ecological components of a hybrid zone in the grasshopper Chorthippus parallelus (Zetterstedt) (Orthoptera: Acrididae). Boletin de Sanidad Vegetal. Plagas (Spain) 20:299–309Google Scholar
  69. 69.
    Giordano R, O’Neill SL, Robertson HM (1995) Wolbachia infections and the expression of cytoplasmic incompatibility in Drosophila sechellia and D. mauritiana. Genetics 140:1307–1317Google Scholar
  70. 70.
    Hartl DL, Clark AG (1989) Principles of population genetics, 2nd ed. Sinauer Associates, Inc., Sunderland, p 682Google Scholar
  71. 71.
    Kelly C, Price TD (2005) Correcting for regression to the mean in behavior and ecology. Am Nat 166:700–707CrossRefGoogle Scholar
  72. 72.
    Wright S (1978) Evolution and the genetics of populations. Vol 4: variability within and among natural populations. University of Chicago Press, ChicagoGoogle Scholar
  73. 73.
    Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freeman & Co. New York. USAGoogle Scholar
  74. 74.
    Christiansen FB, Bundgaard J, Barker JSF (1977) Structure of fitness estimates under post-observational selection. Evolution 31:843–853CrossRefGoogle Scholar
  75. 75.
    Christiansen FB, Frydenberg O, Simonsen V (1977) Genetics of Zoarces populations X. Selection component analysis of the EstZZZ polymorphism using samples of successive cohorts. Hereditas 87:129–150CrossRefGoogle Scholar
  76. 76.
    Knoppien P (1985) Rare male mating advantage: a review. Biol Rev 60:81–117CrossRefGoogle Scholar
  77. 77.
    Hedrick PW (2011) Reversing mother’s curse revisited. Evolution 66:612–616CrossRefGoogle Scholar
  78. 78.
    Noda H, Miyoshi T, Zhang Q, Watanabe K, Deng K, Hoshizaki S (2001) Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): a probable case of interspecies transmission. Mol Ecol 10:2101–2106CrossRefGoogle Scholar
  79. 79.
    Carvajal-Rodríguez A, Rolán-Alvarez E (2006) JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data. BMC Evol Biol 6:40–45CrossRefGoogle Scholar
  80. 80.
    Brommer JE, Gustafsson L, Pietiäinen H, Merilä J (2004) Single-generation estimates of fitness as proxies for long-term genetic contribution. Am Nat 163:505–517CrossRefGoogle Scholar
  81. 81.
    Hood GM (2010) PopTools version 3.2.5. Available online http://www.poptools.org
  82. 82.
    Zug R, Hammerstein P (2015) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev 90:89–111CrossRefGoogle Scholar
  83. 83.
    Champion de Crespigny FE, Butlin RK, Wedell N (2005) Can cytoplasmic incompatibility inducing Wolbachia promote the evolution of mate preferences? J Evol Biol 18:967–977CrossRefGoogle Scholar
  84. 84.
    Engelstädter J, Charlat S (2014) Outbreeding selects for spiteful cytoplasmic elements. Proc Biol Sci 273:923–929CrossRefGoogle Scholar
  85. 85.
    Greenspoon PB, M'Gonigle LK (2014) Host–parasite interactions and the evolution of nonrandom mating. Evolution 68:1558–5646CrossRefGoogle Scholar
  86. 86.
    López-León MD, Cabrero J, Camacho JPM (1996) Negatively assorted gamete fertilization for supernumerary heterochromatin in two grasshopper species. Heredity 76:651–657CrossRefGoogle Scholar
  87. 87.
    Moreau J, Bertin A, Caubet Y, Rigaud T (2001) Sexual selection in an isopod with Wolbachia-induced sex reversal: males prefer real females. J Evol Biol 14:388–394CrossRefGoogle Scholar
  88. 88.
    Jaenike JK, Dyer A, Cornish C, Minhas MS (2006) Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol 4:e325CrossRefGoogle Scholar
  89. 89.
    Arbuthnott D, Levin TC, Promislow DEL (2016) The impacts of Wolbachia and the microbiome on mate choice in Drosophila melanogaster. J Evol Biol 29:461–468CrossRefGoogle Scholar
  90. 90.
    Shropshirea JD, Bordenstein SR (2016) Speciation by symbiosis: the microbiome and behavior. mBio 7(2):e01785–e01715Google Scholar
  91. 91.
    Futuyma DJ (2009) Evolution 2nd Ed. Sinauer Associates, Inc. SunderlandGoogle Scholar
  92. 92.
    Stearns SC, Hoekstra RF (2000) Evolution. An introduction. Oxford Univ. Press, Inc., New York, USA. pp 146–147Google Scholar
  93. 93.
    Dennis AB, Patel V, Oliver KM, Vorburger C (2017) Parasitoid gene expression changes after adaptation to symbiont-protected hosts. Evolution 71(11):2599–2617CrossRefGoogle Scholar
  94. 94.
    Hewitt GM (1993) After the ice—parallelus meets erythropus in the Pyrenees. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 140–164Google Scholar
  95. 95.
    Hewitt GM (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol Ecol 10:537–549CrossRefGoogle Scholar
  96. 96.
    Hewitt GM (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica 139:617–638CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Paloma Martínez-Rodríguez
    • 1
  • Emilio Rolán-Alvarez
    • 2
  • M. del Mar Pérez-Ruiz
    • 1
  • Francisca Arroyo-Yebras
    • 1
  • Carla Carpena-Catoira
    • 2
  • Antonio Carvajal-Rodríguez
    • 2
  • José L. Bella
    • 1
    • 3
    Email author
  1. 1.Departamento de Biología (Genética), Facultad de CienciasUniversidad Autónoma de MadridMadridSpain
  2. 2.Facultad de BiologíaUniversidad de VigoVigoSpain
  3. 3.Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM)Universidad Autónoma de MadridMadridSpain

Personalised recommendations